Science of the Total Environment 757 (2021) 143877 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Interplay of microbial communities with mineral environments in coralline algae Patricia M. Valdespino-Castillo a,1, Andrea Bautista-García b,1, Fabio Favoretto b,c, Martín Merino-Ibarra d, Rocío J. Alcántara-Hernández e, Teresa Pi-Puig e,f, F. Sergio Castillo d, Silvia Espinosa-Matías g, Hoi-Ying Holman a, Anidia Blanco-Jarvio b,⁎ a Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, United States b Laboratorio de Bioingeniería y Ciencias Ambientales (BICA), Departamento Académico de Ingeniería en Pesquerías, Universidad Autónoma de Baja California Sur, La Paz, BCS, Mexico c Gulf of California Marine Program, Scripps Institution of Oceanography, University of California San Diego, CA, United States d Unidad Académica de Biodiversidad Acuática, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico City, Mexico e Instituto de Geología, Universidad Nacional Autónoma de México, Mexico City, Mexico f Laboratorio Nacional de Geoquímica y Mineralogía (LANGEM), Universidad Nacional Autónoma de México, Mexico City, Mexico g Laboratorio de Microscopía Electrónica de Barrido, Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, Mexico HIGHLIGHTS GRAPHICAL ABSTRACT • The interplay of microorganisms and algal mineral bioconstructions remains poorly understood. • Carbonates rich in Fe and Mg found make CA relevant targets to study coastal resilience. • Halophiles and evaporite minerals con- currently suggest halophilic microenvi- ronments in the thallus. • Bacterial microbiota correlated signifi- cantly with temperature and nutrients. • Key bacteria might play relevant roles in adaptive responses of coralline algae. article info abstract Article history: Coralline algae are worldwide carbonate builders, considered to be foundational species and biodiversity Received 30 July 2020 hotspots. Coralline habitats face increasing pressure from human activities and effects related to Global Change, Received in revised form 12 November 2020 yet their ecological properties and adaptive responses remain poorly understood. The relationships of the algal Accepted 12 November 2020 microbiota with the mineral bioconstructions, as well as plasticity and resilience of coralline holobionts in a Available online 3 December 2020 changing environment, are of particular interest. In the Gulf of California, Neogoniolithon trichotomum Editor: Daniel Wunderlin (Rhodophyta) is the main carbonate builder in tidal pools. We performed a multi-disciplinary assessment of the N. trichotomum microstructure using XRD, SEM microscopy and SR-FTIR spectromicroscopy. In the algal Keywords: perithallus, magnesium-calcite and aragonite were spatially segregated and embedded in a polysaccharide ma- Biomineralization trix (rich in sulfated polysaccharides). Mg-calcites (18–19 mol% Mg) were the main mineral components of Biosignatures the thallus overall, followed by iron carbonates related to dolomite (ankerite) and siderite. Minerals of late evap- Coralline rhodophyta oritic sequences (sylvite and bischofite) were also present, suggesting potential halophilic microenvironments Algae carbonates within the algal thalli. The diverse set of abundant halophilic, halotolerant and oligotrophic taxa, whose abun- Halophilic microenvironments dance increase in the summer, further suggests this condition. We created an integrated model, based on envi- Marine microbiota ronmental parameters and the microbiota distribution, that identified temperature and nutrient availability ⁎ Corresponding author. E-mail address: [email protected] (A. Blanco-Jarvio). 1 Denotes equal contribution. https://doi.org/10.1016/j.scitotenv.2020.143877 0048-9697/© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). P.M. Valdespino-Castillo, A. Bautista-García, F. Favoretto et al. Science of the Total Environment 757 (2021) 143877 (particularly nitrate and silicate) as the main parameters related to specific taxa patterns. Among these, Hahella, Granulossicoccus, Ferrimonas, Spongiibacteraceae and cyanobacterial Xenococcaceae and Nostocaceae change sig- nificantly between seasons. These bacterial components might play relevant roles in algal plasticity and adaptive responses to a changing environment. This study contributes to the understanding of the interplay of the pro- karyotic microbiota with the mineral microenvironments of coralline algae. Because of their carbonates with po- tential resistance to dissolution in a higher pCO2 world and their seasonally dynamic bacteria, coralline algae are relevant targets to study coastal resilience and carbonated systems responses to changing environments. © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction Nash et al. (2013) reported that high Mg content carbonates found in CA have higher resistance to dissolution than low Mg-calcites. Coralline habitats are main carbonate builders of coastal environ- Calcarean algal microstructure has been studied with scanning elec- ments facing major transformations due to increasing human activities. tron microscopy (SEM) revealing biomineralizations with complex mi- Pollution, ocean warming and acidification are among the most recog- crostructure (Nash et al., 2019), but only few studies have reported nizable threats for these biodiverse ecosystems (Nelson, 2009; experimental protocols that interlink microbial diversity with algal Hofmann et al., 2014; Cornwall et al., 2019). Understanding the drivers micro-environments. Although their interpretation is often complex, of their diversity, dynamics and resilience are current challenges in the this kind of studies identify holobiontic responses to changing environ- countdown of biodiversity loss related to Global Change. Diversity and mental conditions. Perkins et al. (2016) used high resolution dynamics of biomineralizing holobionts such as corals, sponges or coral- hyperspectral fluorescence to identify an epiphyte micro-spatial gradi- line algae (CA) might provide relevant information to understand the ent along the algal thallus, potentially linked to either pigment varia- building or losing potential of massive mineral bio-constructions, that tion, light gradient, or nutrient availability. Fredericq et al. (2019) ultimately model coastal morphology. Thus, CA and their associated mi- used cryo-SEM microscopy to provide clues to understand the algal crobiota are emergent targets to study the ecology of coralline habitats inner allocation of floridean starch. X-ray microscopy, SEM-EDS and and coastal resilience, carbon cycling and ocean acidification. CA com- microtomography have also contributed to detect taxonomic features plex diversification and evolutionary history are revealed by the ability at microscale, including apical cells morphology and conceptacle char- of this group to colonize a wide range of environmental conditions acteristics (Krayesky-Self et al., 2016). Nash and Adey (2018) used (e.g., high irradiance, high desiccation, oligotrophic conditions; novel protocols with SEM-EDS and field emission scanning electron mi- Hofmann et al., 2018), enabling CA to remain a key component of ben- croscope (FESEM) to describe Mg content differences between internal thic marine communities over geologic time (Aguirre et al., 2000). Much cell-wall and perithallus Mg content (in calcites), in a pioneer attempt is known about coralline algae ecology and physiology, but a major to find the mechanisms that control rhodophyta biominerals diversity focus is needed towards a new understanding of their responses to en- (see also Nash et al., 2013). vironmental changes (e.g., McCoy and Kamenos, 2015). While CA are In this study, SEM microscopy, SR-FTIR spectromicroscopy and min- recognized as biodiverse reservoirs and key coastal carbonate builders, eral determinations by X-ray diffraction (XRD and Rietveld refinement) it is particularly challenging to understand how carbonate structures are used to explore the microenvironments where algae and microbes harbor microbial life and how CA impacts microbial microhabitats. Pre- interact. To explore the interplay of the prokaryotic communities with vious studies have targeted morphogenesis associated with carbonated algal mineral bioconstructions, this study also builds a mechanistic algal thalli (e.g., Cabioch, 1988; Foster, 2001). More recently, the micro- model where Neogoniolithon trichotomum (coralline Rhodophyta) expe- biota and some features of the metabolism of rhodoliths (Sporolithon rienced the seasonality of tropical tidal pools. This seasonality is consid- austral) have been studied from metagenomics-based metabolic pro- ered in a statistical model to select the environmental thresholds files (Cavalcanti et al. 2014 and 2018). However, few studies have inves- associated with prokaryotic abundance. Tidal pools prokaryotic tigated biomineralization-associated structures and their relationship bacterioplankton is analysed to distinguish the prokaryote patterns re- with CA microbiota. lated to the algae. Like in corals, both the vulnerability and resilience of CA depend on their association with symbiotic microorganisms (Reyes-Nivia